Eusociality and Other Sex-Free Lifestyles

Sometimes I hear people making derisive comments towards people who prefer not to have sex, something along the lines of how it goes “against nature” to never have sex, therefore something is horribly wrong with them, etc., etc.

The specific plague I wish upon those unpleasant people is an infestation of termites. Why termites? I’ll talk about that in a bit.

At one point highly social behavior presented kind of a paradox to the traditional, selfish-gene style evolutionary theory. Charles Darwin famously admitted that it was the social behavior of the bee that was going to bring down his entire construction, because most bees- nay, the vast majority of all individual bees spend all their times leading pious, sexless lives centered around helping one other bee reproduce. At the peak of the season, honeybee colonies can have 60,000 nonbreeding individuals- and just one sexually active queen.

Darwin, of course, did not yet know about genes, but he had an inkling that heredity was a clue- that by helping their relatives, the bees were actually helping themselves. Later scientists have filled in more of the gaps using modern molecular science, and yes, from a genetic standpoint, helping a relative is something like helping a piece of yourself.

But at what point does the value of helping close relatives outweigh the value of actually reproducing? That is a question biologists have been grappling with for quite a while. Because in the game of evolution, what matters isn’t how big your species’ population is- what matters is how many of those individuals share your genes.

What is sex, and why do we bother having it?

To understand the value of sexual reproduction, first we have to understand how and why it evolved.

It may surprise you to realize if we just look at species in terms of numbers, the species that never evolved sexual reproduction vastly outnumber the ones who did. Over half the earth’s biomass- that is, the total mass of living things- consists of sex-free prokaryotes. Heck, your own guts contain about ten times the number of bacteria then there are cells in your entire body.

Here’s a tree of all life discovered on Earth. All the sex-havers are squeezed into a portion of that little red section. (“Tree of life int” based on TimVickers‘s work. – Vectorization based on [1], all names in latin for possible usage in different languages.. Licensed under CC BY-SA 3.0 via Wikimedia Commons.)

Now, what most of the organisms that never have sex have in common is the fact that they are unicellular. Unicellular organisms have a great advantage over multicellular organisms via the fact that it is exquisitely easy for them to reproduce. What it means to reproduce is to create a separate individual containing some or all of your own genetic material; and this increase of the same genetic material is what drives evolution in the first place.

I won’t delve too deeply into prokaryotic reproduction, though it is fascinating and very successful. My expertise lies more with multicellular organisms. That said, there are dangers inherent to merely copying your genetic material, as some prokaryotes do by dividing. While division causes the highest proportion of your genetic material to be passed on (100% if there are no errors), perfect copying can actually doom a species. To put it another way, if perfect copying was the only way bacteria reproduced, we wouldn’t keep having to come up with new antibacterials.

It is extremely valuable to frequently introduce new genetic material into your genome, and to have individuals with lots of different genetic combinations present in your species: that way, they are much less likely to all get wiped out by a single environmental factor or event (and hopefully, some of the ones that do survive will also have some of your genes). This is basic biology.

Prokaryotes exchange genetic material with others all the time through the processes of conjugation, transformation, and gene transfer. These processes allow them to easily exchange genetic material not just with members of their own species, but members of a myriad of others. (I really don’t envy the poor biologists that have to delineate between all those different species.)

Okay, so why did sex show up at all, when this great system exists? Well, you can think of sex as kind of a… kind of a 1.2 billion year experiment. Life’s college phase, if you will.

While we can’t consider multicellular organisms more successful that unicellular organisms in terms of sheer numbers, we do have one big advantage over our single-celled cousins: we can specialize within our own species. Our bodies are essentially giant cooperative colonies- hives of cells with identical genetic material. Each cell type has its own task: some make skin, some make organs, some make up the brain, and so on. This level of cooperation wouldn’t be possible if all the cells had different DNA, because out of all these cell types, only one is specialized for reproduction, and only one actually passes on DNA- the gamete. (Egg or sperm to the layperson.)

There are some weird exceptions to this, like Dictyostelium, but ehhhhhh.

Using our creepy living-beehive specialization, we can do all sorts of things like: get really big. Travel much further. Live longer. Think. Release an EP. Etc.

Unfortunately, making most of our individual cells nonreproductive schlubs means that it gets quite a bit more difficult reproduce effectively. And I don’t mean that it’s more difficult to straight up copy our genes. If that were the case, we’d be just fine; in fact, a lot of multicellular organisms can still do this: ever taken a cutting from a plant and replanted it? Watched a hydra reproduce by budding? Or how about reptiles and fish that can reproduce via parthenogenesis? (Look it up!)

What really becomes more difficult is maintaining genetic diversity- that is, recombining genetic material with others to prevent that aforementioned single-disaster-wipes-everybody-out scenario. And here, finally, is where sexual reproduction comes in.

Sexual reproduction utilizes a process called meiosis that acts as a compromise between two parents: each of them gets to put 50% of their DNA into the kid in exchange for what will hopefully be a more vigorous, recombined genome. (Usually 50% and usually two parents, anyway; there are exceptions to basically everything when it comes to genetics.)

With each parent’s genetic output essentially halved per child, you would think that all the members of these species would be having as much sex as they could to make up the difference.

But you’d be wrong.

A Subtler Way of Spreading Your Seed

W.D. Hamilton is a fairly famous evolutionary biologist who came up with a theory called kin selection. (He also lost two fingers while playing with a hand grenade as a child, so you can insert your own “natural selection” joke here.)

Hamilton was one of the first biologists to argue against the idea that sexual reproduction was the only way for animals to ensure the passage of their genes. After all, an organism’s children are not the only ones that share its genes: all of its relatives do, as well, to varying degrees. In fact, in some cases, helping its relatives reproduce might, in some cases, benefit an individual more than trying to reproduce on its own.

He called having your own kids direct fitness, as in you are directly passing on your genes, and helping your relatives indirect fitness, as in “I assume these people carry some of my genes.”

This is summed up in what is known as Hamilton’s rule. Roughly, it’s an equation that determines the value of a seemingly “altruistic” act based on how related two individuals are. A third cousin, for example, might not share many of your genes, but your sister would share a whole lot; therefore, it’d be worth your while to help her out.

The symbol r stands for the coefficient of relationship, or the degree of relatedness between two individuals, with 1 referring to two individuals with the exact same genetic material and 0 referring to two individuals sharing no genes.

So, your relationship to each of your biological parents (assuming that there are no chimeras involved) is r = .5. Here’s a diagram looking at some more r-values in familial relationships:

This figure assumes that there’s no degree of relatedness between your parents and nobody’s a chimera and that all parties are diploid.

If you’re looking at this in a purely clinical, cold-hearted scientist fashion, it would make the most sense to help your children because they share a high theoretical percentage of your genes and their offspring will have a greater percentage of your genes then, say, your siblings’ offspring.

However, there are plenty of circumstances where it might be more beneficial to throw your resources into other family members beside your direct descendants. Imagine you are the oldest child, trembling just on the cusp of adolescence. You could move out right away and try to get breedin’ on your own, but mortality for young and inexperienced idiots like you is incredibly high. Rather than risking it all so soon, you could increase your genetic output substantially by helping your parents raise your (r = .5) siblings until you are ready.

This isn’t just theoretical; it’s a common practice in many social species, especially monogamous ones. Gray wolves do it, great tits do it.

Living in groups fosters a degree of kin selection (though that’s not to say that solitary animals don’t go slightly easier on their offspring during territorial disputes). For starters, your kin are right there, easy-access. But a lot of animals live in groups because life would be much harder alone, either in acquiring prey, fending off kleptoparasites or predators, or just raising young. The harder life is alone, the more sense it makes to help your relatives for a while; because you just can’t have children if you’re dead.

This is social behavior. Eusocial behavior is when those kids just never move out.

The Perils of Eusociality: 60,000 Asexual Bees

Eusociality is the pinnacle of social behavior; you just can’t get any more cooperatively social than a eusocial organism. The simplest eusocial societies are divided into reproductive and nonreproductive castes; the most complex have many more castes that cannot survive without one another.

A good example of this would be termites: not only do the workers and soldiers depend on queens and males to do their breeding for them; the workers and soldiers depend on each other. The workers depend on soldiers for protection, obviously, and soldiers depend on workers to feed them because in some species their jaws are so large that they cannot feed themselves.

Most of us are familiar with eusocial insects: many species of ants, bees, wasps, and all species of termites form eusocial colonies. However, eusociality has evolved independently in several other groups of insects, including aphids, thrips, and weevils. Eusociality has also been identified in one species of shrimp (Synalpheus regalis) and two species of mammals, the naked mole rat and the Damaraland mole rat.

We can infer two things from this sporadic appearance of eusocial behavior: one, since it evolved independently in multiple species, even across phylums, it must be very beneficial; two, since it evolved only a few times overall in all these phyla, it must only be highly beneficial in certain circumstances.

So what might these circumstances be?

Well, to start with, most eusocial species have a few factors in common, factors that helped facilitate their group-living lifestyle to begin with. These factors are:

Highly altricial young that have low chances of survival with only one or two parents in attendance

Food resources that are patchily distributed, but found in excess where they do exist. For example: a tree for termites, massive tubers for naked mole rats, fungi for leafcutter ants, flowers for bees. These resources facilitate the aggregation of large numbers of individuals in small areas.

However, a hallmark of many species that favor patchily-distributed resources is extreme territoriality. Hummingbirds, for example, are so aggressive in defending their flower patches that they will attack potential mates. There has to be a reason that eusocial animals are able to group together and cooperate without infighting, and that reason probably has something to do with a high degree of inclusive fitness. (No, shut up, E. O. Wilson.*) But how do eusocial species achieve this?

Our pal Hamilton came up with his own theory for this: haplodiploidy. It’s probably the one you were taught about in college if you ever studied eusocial insects (I know firsthand that it was being taught at my alma mater as recently as 2012!) However, problems with this theory were first brought up in 1998, and in the scientific community at large it’s considered more of a possible side effect than a major evolutionary driving force behind eusociality.

Still, I’ll go over it briefly, because it still does have some bearing on how some eusocial species behave. Just not nearly as much as Hamilton thought.

The Boom and Bust of Haplodiploidy

Ploidy refers to the number of chromosome pairs each individual has. For example, haploid cells contain one set of chromosomes, while diploid cells contain a pair of each chromosome. Most plants and fungi can switch between haploid and diploid states, but the only animal cells that are usually haploid are our gametes- our sperm and eggs. These contain one set of chromosomes because they are intended to combine with another gamete- this is where the 50-50 genetic compromise between parents occurs.

Hamilton noticed that quite a number of eusocial insects employed a usual chromosomal system in which females were diploid, but males were haploid. This radically changed the relatedness of each member of the colony.

How? Because instead of getting half the male’s genes, the daughters were getting all of them, along with half of their mother’s genes. Since most eusocial queens can essentially hang on to sperm indefinitely, they can produce thousands of these daughters.

(Sons, however, come from unfertilized eggs containing one-half of the mother’s genetic material, meaning they have no fathers and cannot have sons, but are related to their grandfathers and grandsons. Weird!)

If you plug all that into the formula to get relatedness, you find that while r between mother and daughter equals .5 as usual, r between sisters equals the startlingly high .75.

In effect, sisters were more related to each other then they were to their mother. In Hamilton’s mind, this unusually high degree of shared genetic material was greater impetus for sisters to behave altruistically towards each other rather than try to breed themselves- though they would also be very eager to raise sisters that might eventually become queens in their own right because of this relatedness.

At first glance, this seems like a really solid theory. But there are two major, glaring problems:

Not all eusocial species are haplodiploid (termites, naked mole rats, etc.), and there are many non-eusocial species that are haplodiploid as well (various solitary hymenopterans).

This theory only holds up as long as a queen only mates once (i.e., all her daughters have the same father). But in many eusocial species, the queen mates with multiple males. This results in half-siblings that are only related by a coefficient of .25.

So, while haplodiploidy might be a definite bonus in certain eusocial societies (indeed, worker honeybees are more likely to try and make their sisters into queens when their mother has only mated once, and it works okay in monogamous species), it doesn’t hold up as an evolutionary reason behind eusociality’s entire existence.

The answer to what actually does prompt a species to evolve eusocial behavior is currently met with a cough and a shuffling of feet in the scientific community. There are some other theories with fairly solid evidence, but it seems as though the real answer is going to be much more complex than Hamilton’s neat little chromosomes.

Did all eusocial species evolve from monogamous ancestors?

I mentioned before that the haplodiploidy theory might work for species that had an ancestral monogamous state, so that mom originally only mated with one male ever. (I also mentioned that she only needs to mate with this male once- she just hangs onto his sperm and lets him die. Ultimate sexual loyalty!)

In this case, even if the species later evolved away from monogamy, they were still stuck with their eusocial tendencies; it’d be extremely hard for the more or less helpless queens to cut ties with their workers and live on their own, or for the workers to suddenly start breeding again (well, for most species; some sterile workers can revert to a reproductive state, but then they’d run into the same problems the queen did). Evolutionarily, they’d be backed into a corner, unable to live in any manner buteusocially.

But even for non-haplodiploid eusocial species, the monogamy theory has some merit. Most termite species, for example, function with both a queen and a king, with male and female sterile workers. The queen and king are generally a monogamous pair, the workers their offspring, which are all related by r = .5, rather than a half-sibling’s r = .25.

This theory is receiving some good support as studies expand on it; it seems that the eusocial shrimp are confirmed faithful partners to one another, for example. And while eusocial mole rat queens may have up to three sexual partners, the other, non-eusocial species of their genera are monogamous.

So monogamy may be a definite precursor for the evolution of eusociality, due to the fact that it facilitates high degrees of sibling relatedness. However, as there are many monogamous species that aren’t eusocial, it definitely isn’t the only factor.

The Possible Importance of Inbreeding

If you’re a devious-minded person, you may have looked at that r-value figure up there and wondered what would happen to those little numbers if, say, you were to have sex with your cousin.

It’s ok. Judgement-free zone here. My grandparents on one side were third cousins, after all; we can’t all claim to have perfect r-values in our lineage.

As a matter of fact, inbreeding may play a large role in the formation and maintenance of eusocial societies. As your sneaky little brain may have guessed, keeping the love within the family does lead to higher r-values, though at the risk of accruing the effects of inbreeding depression. Heck, if done really religiously, it can lead to r-values higher than the much-touted .75 that haplodiploid sisters get.

As you would expect, inbreeding is quite prevalent among some, but not all eusocial species. Naked mole rats are major inbreeders due to the fact that they have very limited dispersal from their natal nest. (This has to do with the availability of their food, which grows patchily, and their dislike of direct sunlight.) It is estimated that most naked mole rat matings occur either between parent and offspring or full siblings. One study found that on average, naked mole rat siblings are related by a factor of .81.

Who would have guessed that this beautiful animal is inbred?

When you’re that closely related to your brothers and sisters- much more closely than you would be to your own offspring- it’s almost no issue giving up your own reproductive rights to allow mom to make more of them. That’s just basic math.

However, the same is not quite true for the naked mole rat’s relatives, the Damaraland mole rats. It’s important to note that eusociality likely evolved separately in these two species as well! The Damaraland mole rats are obligate outbreeders, meaning that they will refuse to breed with anybody but a foreigner. Even if the queen is removed, the female that takes her place won’t begin breeding until a foreign male comes along to mate with her.

The lesser-known but equally lovely Damaraland mole rat prefers not to mate with family members. (Source.)

Aside from close inbreeding, there’s another factor that leads to heightened relatedness in many eusocial species: the fact that even when breeding individuals disperse, they tend not to disperse very far from their nest sites. This is due to the aforementioned patchy nature of their food supplies, but also because their breeders are often poorly equipped to survive on their own. Some breeders travel with a compliment of workers, such as when honeybees swarm, but this also limits the distance they can travel.

The reduced rate of dispersal means that even if species like Damaraland mole rats prefer to mate with outsiders to reduce the rate of inbreeding, the outsiders may actually still be somewhat closely related to them. These types of populations are referred to as viscous populations, and they’re often cited as a reason why a species might become less aggressive overall to members of its own kind: there’s a chance that any given stranger is still carrying a lot of its genes.

Ultimately, eusocial species are successful where they arise, but only in very specific niches, and with significant costs: they lose a large amount of genetic diversity, need large amounts of food to support their high numbers, and cannot revert back to a less social state once locked in.

Is There Such a Thing as a Pre-Eusocial Species?

A colony of termites might have millions of nonbreeding individuals compared to a handful of breeders, a factor that is too many decimal points gone to bother trying to express as a percentage. Even the mole rats, mammals with slightly more limited reproductive capabilities than insects, maintain a reproductive population of only 1-8% in their entire species.

These numbers are impressive, and representative of what are known as truly eusocial species. But they are not the only species where the nonbreeding individuals greatly outnumber the breeders.

This is true for many species of mongoose, for example, with one of the most extreme being the meerkat. Colonies of 20-50 individuals usually have a single breeding pair, and though some members may eventually disperse to breed, about 70% of individuals reach sexual maturity and choose to stay with the group their whole lives.

A very similar social pattern is found in African wild dogs. Much like true eusocial species, African wild dogs are rarely successful parents unless they have more group members to help care for their massive litters of up to twenty puppies. In fact, studies suggest that African wild dog groups will fail unless they contain more than four individuals; in this way, they are obligately social. Like mongooses, relatively few African wild dogs end up breeding- they even disperse in same-sex groups, where only one member (the queen or king?) will breed, with the others (the workers?) submissive to them.

The degree of sociality in African wild dogs have even led some experts, such as Scott and Nancy Creel, to argue that they are actually eusocial, or at least heading that way; but since they don’t have a clear separation of reproductive/nonreproductive castes, this is dubious.

Still, it may be that in highly social species, far fewer members breed than we might expect.

Family Isn’t Everything

Kin selection does not explain every single incidence of nonbreeding animals. Two studies on the sexual behavior of rams found that 2-3% of rams never attempted to mate with anybody; furthermore, these “asexual” fellows had perfectly normal sexual hormone levels. It shouldn’t need to be stated that sheep don’t follow the hallmarks of eusocial or even pre-eusocial species: they aren’t monogamous, they have spread resources, and they certainly don’t form castes.

I’ve been unable to find any other studies on asexual behavior in a non-inclusive fitness basis, but that doesn’t mean they don’t exist. Asexual behavior is hard to study in animals because a scientist who observes adult animals not mating probably assumes they’ll be mating at some other time, or that they are sick, or that they are a reproductively suppressed subordinate, or a whole host of other reasons finally leading up to an inherent lack of sexual desire.

However, I do think that more data will eventually turn up; we’ve seen how successful asexual individuals can be in eusocial societies, and more and more research points to the benefits of homosexual behavior- I expect we will find many more animal societies where asexual behavior is both common and successful.

I should be clear that I don’t intend for this article to be a validation for asexual humans- for one thing, humans aren’t termites or mole rats or sheep, and for another, you certainly don’t need the validation of me or anyone else for your identity.

Bonus: here’s an actual exam question I had to answer on an actual college exam about inclusive fitness.

The answer is that his parents are dead. (Click for larger view.)

Wasn’t that lack of sex exciting? If you need a break from the hot n’ heavy platonic cuddling, you can read posts about animals actually doing the do, like this one on animal masturbation and this one on homosexual birds. For some animals that are really desperate to impress, here’s an article on chase-away sexual selection!

To view a list of all my animal articles, head to the Nonfiction section.

One Comment

Thinking about that test question there are I believe a few factors to go through. First are we assuming here the Bruce Wayne Batman since both Gotham and Joker are mentioned. This would mean your mother has been already long dead, and your stepfather some kind of necrophiliac/necromancer. Probably not the most savory fellow. This would also mean the step-brothers are some kind of zombie hell-spawn most likely. This brings in the ethics of whether they shouldn’t be activity killed or would such a union be capable of leading a fruitful life/un-life. Either way a genetic connection would be severely warped in an case. The first room seems to have with dead mother, unrelated father and unnatural offspring at best a level of 0. Second room it might be important to establish who the wife, though the most likely would be Talia Al-ghul. This would imply Damien identifying as transgender( and hopefully Bruce is a supportive father) but leaves the mystery of the second daughter. I feel there is a strong possibility might be imaginary. As any offspring would also carry a quarter of Ra’s’ genes which in the long run could be very detrimental. The sister is most likely Ra’s himself in a clone body of Talia, because that’s just the kind of schemes he’d be up to. So here we have one child at .5 (and honestly should lose .125 for Al ghul genes), or a total of around .375. Clearly Batman should stay home and brood about how he was unable to save his family, not risking his own life and losing any future possibilities of passing on his genes. Terry McGinnis made a pretty good Batman himself after all. Its fun to over think test questions!
P.s. thanks for sharing your test mistakes with us.